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Originally published as JCO Early Release 10.1200/JCO.2005.12.107 on February 22 2005 © 2005 American Society of Clinical Oncology. Late Referrals to Specialized Palliative Care Service in JapanFrom the Department of Palliative and Supportive Care, Palliative Care Team and Seirei Hospice, Seirei Mikatabara Hospital; Palliative Medicine, Shizuoka General Hospital, Shizuoka; Department of Psychiatry, Nagoya City University Medical School, Nagoya; Psycho-Oncology Division, and Psychiatry Division, National Cancer Center Research Institute East, Chiba; Hospice, Yodogawa Christian Hospital, Osaka; Institute of Clinical Medicine, University of Tsukuba, Ibaragi; Hiroshima Palliative Care Promotion Center, Hiroshima; Department of Internal Medicine and Palliative Care, The Cancer Institute Hospital, Japanese Foundation for Cancer Research, Tokyo; Department of Palliative Medicine, Tohoku University Hospital, Miyagi; Palliative Care Unit, Kawasaki Social Insurance Hospital, Kanagawa, Japan Address reprint requests to Tatsuya Morita, MD, Department of Palliative and Supportive Care, Palliative Care Team and Seirei Hospice, Seirei Mikatabara Hospital, 3453 Mikatabara-cho, Hamamatsu, Shizuoka 433-8558, Japan; e-mail: seireihc{at}jt6.so-net.ne.jp
PURPOSE: To clarify the bereaved family's perceptions about the appropriateness of timing when physicians first referred patients to palliative care units, and to identify the factors contributing to family-perceived late referrals. SUBJECTS AND METHODS: A multicenter questionnaire survey was conducted on 630 bereaved family members of cancer patents who were admitted to palliative care units in Japan. A total of 318 responses were analyzed (effective response rate, 62%). RESULTS: Half of the bereaved family members regarded the timing of referrals to palliative care units as late or very late, while less than 5% of families reported early referrals (very late [19%, n = 59], late [30%, n = 96], appropriate [48%, n = 151], early [1.6%, n = 5], and very early [2.2%, n = 7]). Multiple regression analyses revealed that the independent determinants of family-perceived late referrals were: family belief before admission that palliative care shortens the patient's life, insufficient in-advance discussion about preferred end-of-life care between patients/families and physicians, families' insufficient preparation for changes of patient conditions, and hospital admission before referrals. CONCLUSION: In Japan, the timing of referrals to palliative care units was late or very late from the families' perspectives. The independent determinants of family-perceived late referrals were: family misconception about palliative care, inadequate communication with physicians, and families' insufficient preparation for deterioration of patients' conditions. Systematic strategies to overcome these barriers would contribute to providing appropriate palliative care at all stages of cancer.
The WHO defines palliative care as "an approach that improves the quality of life of patients and their families facing the problems associated with life-threatening illness," and states that this is achieved "through the prevention and relief of suffering by means of early identification and impeccable assessment and treatment."1 Although palliative care is rooted in compassionate care for dying patients, the primary aim of palliative care is to minimize patient and family suffering at all stages of life-threatening illness.1 Early referrals to specialized palliative care service, that is, immediate referrals to palliative care specialists when patient and family require specialized care for adequate symptom relief, could be useful in achieving this goal through early and systematic detection of unmet needs, prevention of symptoms, and strengthening emotional connections between patients and families.2-5 Specialized palliative care service includes home-based hospice care programs, inpatient hospices, palliative care units, and palliative care teams. In the United States, home-based hospice care programs are a common form of specialized palliative care, and several studies have revealed that physicians usually refer patients to hospice care programs at very late stages of cancer. While a nationwide survey of American internists revealed that the mode of best time of referrals to hospice was 13 weeks before death (73%),6 the median survival from the initial referral to hospice to patient death ranged from 4 to 5 weeks, and approximately 15% of the patients died within a week after enrollment in hospice care programs.7,8 Surveys from the United States, Italy, and Japan have consistently shown that physicians referred patients to hospice care programs or palliative care units at the very latest stage of cancerthe median survival from the initial referral to patient death ranged from 3 to 6 weeks, and approximately 15% of the patients died within a week after initial referrals.9-11 A shorter length of stay was associated with less satisfaction with palliative care by family caregivers, and lack of adequate time could lead to poor symptom control.9,11 Theoretically, the factors contributing to late referrals are associated with patients, families, physicians, and health care systems.11-15 To date, several empirical studies on health care providers have identified some barriers to early referrals: patients/families' unwillingness to receive palliative care, patients/families' misconceptions about palliative care, physicians' unwillingness to discuss end-of-life care, and lack of palliative care services available.12-16 Although these findings provide useful information to understand why physicians do not refer patients to specialized palliative care services at an earlier stage of cancer, they are ultimately based on physicians' reports, and no systematic studies have been performed to directly collect patients' or families' views. The primary aim of this study was thus to clarify the bereaved family's perceptions about the appropriateness of timing when physicians first referred patients to specialized palliative care services, and to identify the factors contributing to the perceived late referrals. In Japan, the Ministry of Health, Labor and Welfare has strongly supported dissemination of specialized palliative care services, with coverage of palliative care units by National Medical Insurance since 1991, and the number of palliative care units having dramatically increased from only 5 in 1991, to 123 in 2004. To be approved as a palliative care unit, institutions must fulfill the requirements of the Ministry of Health, Labor and Welfare, including standards for the number of staff, the facility, and the equipment. Palliative care units are called either "palliative care units" or "hospices," depending on the religious background, but their roles are the essentially sameintensive symptom control and end-of-life care are simultaneously provided. The majority of palliative care units belong to general hospitals and have interdisciplinary teams including attending physicians, nurses, and other specialists.11,17 On the other hand, the growth of home-based specialized palliative care programs has been slow,18,19 and palliative care teams were not covered by National Medical Insurance until 2002. Therefore, the most common type of specialized palliative care service in Japan is the palliative care unit, and we chose palliative care units as study targets for this investigation.
Methods This was a cross-sectional anonymous multicenter survey of the bereaved families of cancer patients who had been admitted to palliative care units in Japan. We mailed questionnaires to bereaved families in August 2003, and again in October 2003 to nonresponding families. If the families did not want to participate in the survey, they were requested to return a questionnaire with "no participation" indicated, and the second questionnaire was not mailed. We initially identified 19 palliative care units as potential participating institutions, following the inclusion criteria: (1) approved by the Japanese Association of Hospice and Palliative Care Units, (2) belonging to a general hospital with more than 300 beds, and (3) having 20 or more beds and treating 100 or more patients in 2001. We then approached 11 palliative care units with collaborative researchers available. There were no statistically significant differences in the number (± standard deviation [SD]) of inpatient beds, the number of patients, or administration periods between the included and excluded institutions (22 ± 2.5 v 23 ± 3.1, P = .39; 161 ± 33 v 183 ± 65, P = .40; 41 ± 5.8 v 42 ± 13, P = .80; respectively). Ultimately, nine units agreed to participate in this survey. All institutions had bereavement programs (individual follow-up with telephone and/or letter, n = 9; system for consultation with mental care professionals, n = 7; supportive groups or meetings of the bereaved, n = 5).
Subjects Primary physicians identified the potential participants following the inclusion criteria: (1) bereaved family members of an adult cancer patient (one family member was selected for each patient), (2) age 20 or older, (3) capable of replying to a self-reported questionnaire, (4) awareness of the diagnosis of malignancy, and (4) no serious psychological distress recognized by the primary physicians. The last criteria were adopted on the assumption that primary physicians could identify families who would suffer serious psychological burden from this survey because they cared for the families closely in inpatient care settings, with a mean admission period of 47 days (the Japanese Association of Hospice and Palliative Care Units, unpublished data, 2002). Each hospital was requested to consecutively enroll 70 families of the patients who died in 2001. Completion and return of the questionnaire was regarded as consent to participate in this study. The ethical and scientific validity were confirmed by the institutional review board of each hospital.
Questionnaire Primary physicians recorded patient backgrounds (age, sex, primary tumor site, and actual admission periods). The families reported their age, sex, relationship to patient, intervals from diagnoses to death, interval from patient death to study, anticancer treatments the patient had received and their informed aims, and waiting periods from application to admission to palliative care units. The primary end point was family-perceived appropriateness of the timing when physicians first referred patients to palliative care units. The level of the family-perceived appropriateness was rated on a 5-point scale as "should have been referred much later (very early)," "should have been referred a little later (early)," "referred at the appropriate time," "should have been referred a little earlier (late)," and "should have been referred much earlier (very late)." In addition, we requested that families report what the patients described about the appropriateness of the referral timing, on the same scale. The families were further requested to report 23 factors potentially contributing to the perception about the timing of referrals. The factors were conceptualized prior the survey based on literature review and expert discussions,2-15 and were classified into nine categories: (1) seven demographic variables (patient age, sex, intervals from diagnosis to death; responding family member age, sex, relationship to the patient, interval from patient death to study); (2) six variables related to impressions of palliative care units; (3) two variables concerning information (availability of a counseling section/staff, or presence or absence of a relative or family member who had been admitted to a palliative care unit); (4) treatment settings before the admission to palliative care units (home or hospital); (5) two variables related to in-advance discussion (whether patients and families, or patient/family and physicians sufficiently discussed preferences regarding end-of-life care); (6) two variables concerning patients' needs (presence or absence of distressing physical symptoms just before referral, and whether patients willingly wished for referral to palliative care units); (7) patients/families' concerns about continuity (examined by the degree of agreement of the statement "I strongly wished to be treated by the same physician" on a 5-point Likert-type scale of 1: disagree, to 5: strongly agree); (8) patients/families' wishes for continuing treatments (examined by the degree of agreement with the statement "I strongly wished for the treatments to be continued" on a 5-point Likert-type scale of 1: disagree, to 5: strongly agree); and (9) patients/families' preparation (examined by the degree of agreement of the statement, "I was not sufficiently prepared for the changes in the condition" on a 5-point Likert-type scale of 1: disagree, to 5: strongly agree). To evaluate the impressions of palliative care units before and after admission, we used the degree of agreement of six statements on a 4-point Likert-type scale of "1: disagree," "2: slightly disagree," "3: agree," and "4: strongly agree": (1) alleviates pain, (2) support patients in living with dignity, (3) a place where people only wait to die, (4) provides no medical treatments, (5) shortens the patient's life, and (6) expensive. Moreover, the families were requested to report how actual care they received in palliative care units was different from their first impressions: much worse, worse, just like the initial impression, better, and much better. In addition, if the families reported that in-advance discussion about preferred end-of-life care between patients or families and physicians was insufficient, they were requested to choose the main reasons from patient unwillingness, family unwillingness, or physician unwillingness. Also, they rated the degree of necessity for improvement in care they had received before admission to palliative care units from "no," "some," "considerable," or "much improvement" needed. Finally, the respondents were requested to rate how they thought palliative care physicians would have been helpful if they had participated in patient care earlier ("great help," "considerable help," "some help," or "little help"). Furthermore, the respondents rated the perceived efficacy of 10 strategies to help patients and families in earlier referral to palliative care services earlier on a 3-point Likert-type scale of "not useful," "useful," or "very useful."
Analyses
We initially screened 23 potential contributing factors by univariate analysis. Univariate analysis was performed using Student's t test and the To examine the changes in the impressions of palliative care units after admission, the degree of agreement on six statements was compared before and after admission using Student's paired t-test. To investigate the changes in negative impressions, the degree of agreement was compared before and after admission separately for families who agreed or strongly agreed that palliative care "provides no medical treatments" and "shortens the patient's life." All analyses were performed using the Statistical Package for the Social Sciences (version 11.0; SPSS Inc, Chicago, IL).
Of 630 families considered as potential participants, 38 families were excluded due to serious psychological distress recognized by primary physicians (n = 22) or lack of available competent adult family members (n = 16). Of 592 questionnaires sent to the families, 26 were returned as undeliverable, and a total of 374 families returned questionnaires (response rate, 66%). Of them, 13 families refused to participate, and 43 responses were excluded due to missing data in primary end points. Thus, 318 responses were finally analyzed (effective response rate, 62%; 318 of 510). Table 1 summarizes the backgrounds of the patients and family members. The anticancer treatments the patients had received in the 6 months before admission to palliative care units were: surgical treatment (28%, n = 90), chemotherapy under hospitalization (46%, n = 145), chemotherapy at home or outpatient services (42%, n = 134), radiation therapy (33%, n = 106), and none (18%, n = 58). The informed aims of these treatments were: cure of cancer (6.0%, n = 19), prolongation of survival period (34%, n = 108), symptom palliation (47%, n = 148), and none (6.6%, n = 21).
Before being admitted to palliative care units, 176 patients (55%) had been admitted to hospitals, 101 patients (32%) were treated at outpatient services, and 36 patients (11%) had received home care service. Before admission, 270 patients (85%) had distressing physical symptoms, and 50% (n = 126) reported that considerable or much improvement was necessary in the care they had received before admission to palliative care units; 18% (n = 57) stated that no improvement was necessary. Based on the family reports, 138 patients (43%) willingly wished for referral to palliative care units. Also, 196 families (62%) reported that a counseling section/staff was available, 49 (15%) had a relative/friend who had been admitted to a palliative care unit, and 167 (53%) reported that they had sufficiently discussed preferred end-of-life care in advance with patients.
Family-Reported Appropriateness of the Timing of Referrals
Among 138 families who reported what patients had said about the timing of referrals, 59% reported the patients said the timing of referral was late or very late (very late [24%, n = 33], late [35%, n = 48], appropriate [36%, n = 50], early [2.2%, n = 3], and very early [2.9%, n = 4]). The concordance between families' and patients' evaluations was moderate (Cohen's
The mean (± SD) admission period at palliative care units was 34 ± 39 days (median, 22 days), and 17% (n = 54) and 35% (n = 111) of the patients died within 1 week and 2 weeks, respectively. The admission periods were not significantly linearly correlated with family-perceived appropriateness of the timings of referrals (
Determinants of Family-Reported Late Referrals
Multiple logistic regression analyses revealed that the independent determinants of family perception of late referrals were: family belief before admission that palliative care shortens the patient's life, insufficient in-advance discussion about preferred end-of-life care with physicians, families' insufficient preparation for changes of patient conditions, and treatment settings before admission (hospitals; Table 3). In another model in which "families' insufficient preparation for changes of patient conditions" was excluded, "patients' insufficient preparation for changes of patient conditions" was an alternative significant determinant for family-perceived late referrals.
Changes in Impressions of Palliative Care Units Table 4 presents the changes in families' impressions of palliative care units before and after admission. The degree of agreement on the statements "alleviates pain" and "support patients living with dignity" significantly increased after admission, and the degree of agreement on the statements "a place where people only wait to die" and "expensive" significantly decreased.
By separate analyses on 157 and 73 families who agreed or strongly agreed that palliative care "provides no medical treatments" and "shortens the patient's life" before admission, respectively, the degree of agreement (± SD) on each statement significantly decreased from 3.2 ± 0.40 to 2.8 ± 0.85 (P < .001), and 3.2 ± 0.43 to 2.6 ± 0.97 (P < .001), respectively. In addition, among 257 families who reported they had received some information about palliative care units from treating physicians before use of palliative care units, 39% (n = 101) and 30% (n = 76) reported that care they actually received in palliative care units was much better and better than the initial impression, respectively, while 4.7% (n = 12) reported that actual care was worse.
Family-Reported Reasons of Insufficient in-Advance Discussion About Preferred End-of-Life Care With Physicians
Recommendations From Families to Enable Patient and Families to Achieve Earlier Referral to Palliative Care Services
This is, to our knowledge, the first study to investigate the family-perceived appropriateness of the timing of referrals to palliative care unitsspecialized types of palliative care services. One of the important findings of this study was the clarification of the proportion of families who considered that the timing of referrals was late, appropriate, or early. Half of the bereaved families surveyed regarded the timing of referrals as late or very late, and less than 5% reported it as early. In addition, the median admission period was less than 1 month (22 days), and approximately 20% of the patients died within 1 week. This finding is compatible with existing literature7-10 and strongly suggests that the timing of referrals to specialized palliative care services, including palliative care units, inpatient hospices, and home-based palliative care programs, is likely to be delayed. It is noteworthy that admission periods were only moderately correlated with family-perceived appropriateness of the timing of referrals. This finding strongly suggests that it is not the admission period itself, but rather patient and family perceptions about timely consultation to specialized palliative care services, that should be included as a indicator for appropriate use of palliative care resources in future studies. The second and the most important finding was the clarification of barriers to appropriate referral to palliative care units. These barriers include family belief before admission that palliative care shortens the patient's life, insufficient in-advance discussion about preferred end-of-life care with physicians, families' insufficient preparation for changes in patient condition, and treatment settings (hospitals). However, negative impressions about palliative care units markedly improved after admission. Furthermore, the families listed physicians' unwillingness as the main reasons for insufficient in-advance discussion about preferred end-of-life care, rather than patients' or families' unwillingness. These findings confirmed preliminary results from qualitative and small quantitative studies that the barriers to appropriate referrals were patients' or families' misconceptions about palliative care, poor in-advance discussion about preferred end-of-life care due to physician unwillingness, and patients' or families' unwillingness to accept terminal conditions.11-15 To overcome the first barrier related to misconceptions about palliative care, providing accurate information about palliative care to both oncologists and lay persons via systematic educational programs, distribution of pamphlets, or mass media would be useful. To overcome the second barrier (insufficient in-advance discussion about end-of-life care with physicians), it may be valuable to implement a special hospital section where patients and families can consult about palliative care, arrange for patients and families to see palliative care physicians earlier, and educate oncologists about specific skills for communicating preference in end-of-life care in earlier stages. To overcome the third barrier related to patients' or families' insufficient preparation for fatal conditions, allowing patients to receive desired medical treatments in palliative care units and intensive psychological support for patients and families throughout the clinical course may be beneficial. This survey was performed on bereaved family members, and this accounts for both the strengths and limitations of this study.22 Compared with a patient survey, the strength is that we could obtain information about patients with poor general conditions who could not reply themselves to a questionnaire survey. The limitation is that, as the concordance of patients' and families' evaluations was moderate, the findings could not be straightforwardly applied to patients. Compared with surveys of families receiving ongoing care, the strength is that bereaved families could evaluate the appropriateness of timing of referrals from the viewpoint of the whole clinical course of patients. The limitation is that, as evaluations were made retrospectively after patient death, the findings might be influenced by recall bias and bereavement, such as depression, self-blame, or guilt. Because no single study could reach a definite conclusion due to the intrinsic limitations in each study, the findings of this study should be interpreted together with future studies on patients and families receiving ongoing care. This study had several limitations. First, as 3.5% of families who had serious psychological distress as determined by primary physicians were excluded and the response rate was not very high (62%), the population might not be representative of the study subjects. Second, we could not enroll all potential institutions for this study. We do not believe, however, that this seriously influenced the conclusions because of the absence of significant differences in institutional backgrounds and the sufficiently large number of subjects studied. Third, the study subjects were limited to the families of patients who had been admitted to palliative care units, and the findings might not be applicable to families in other settings. In conclusion, half of the Japanese bereaved families receiving inpatient specialized palliative care services regarded the timing of referrals as late or very late, while less than 5% reported it as early. The independent determinants of family perception of late referrals were family belief before admission that palliative care shortens the patient's life, insufficient in-advance discussion about preferred end-of-life care with physicians, families' insufficient preparation for changes of patient conditions, and treatment settings (hospitals). Systematic strategies to overcome these barriers should be explored to achieve appropriate referrals to specialized palliative care services.
The authors indicated no potential conflicts of interest.
Supported by a Health and Labor Sciences Research Grant for Clinical Research for Evidenced Based Medicine. Authors' disclosures of potential conflicts of interest are found at the end of this article.
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Copyright © 2005 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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